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Animal Behaviour
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Review
Food-associated vocalizations in mammals and birds: what do these calls
really mean?
Zanna Clay a, *, Carolynn L. Smith b, Daniel T. Blumstein c
a
Living Links, Yerkes Primate Center, Emory University, Atlanta, GA, U.S.A.
Department of Biological Sciences, Macquarie University, Sydney, NSW, Australia
c
Department of Ecology and Evolutionary Biology, University of California, Los Angeles, U.S.A.
b
a r t i c l e i n f o
Article history:
Received 14 August 2011
Initial acceptance 4 October 2011
Final acceptance 4 November 2011
Available online xxx
MS. number: ARV-11-00652R
We dedicate this paper to the memory of
Professor Chris Evans, a scholar and friend
who thought hard about the meaning of
animal signals
Keywords:
alarm call
food-associated call
referential signalling
status signalling
Alarm calls and food-associated calls from a diverse range of species are said to be functionally referential, in that receivers can use these sounds to predict environmental events in the absence of other
contextual cues. The evolutionary driver for referential alarm calls has been hypothesized to be the
mutually incompatible escape behaviours required to avoid different predators. However, some species
produce acoustically distinctive and referential alarm calls but do not show highly referential abilities in
other domains. We examined whether food-associated calls in many species are likely to be functionally
referential and whether they specifically communicate about characteristic features of food. Foodassociated calls are given in both feeding and nonfeeding contexts, and the types of information contained vary greatly. Most species do not produce unique calls for different foods; more common is
variation in the call rate, which suggests that call structure reflects the callers’ internal state rather than
the food type. We also examined the ultimate function of food-associated calls to evaluate whether there
is a unifying explanation for the evolution of functionally referential food calls. Based on the literature,
there does not appear to be a unifying function. In conclusion, while functionally referential foodassociated calls have been convincingly demonstrated in a few species, it is more common for these
vocalizations to reflect arousal rather than additionally providing specific referential information about
the feeding event. At this point, there is no compelling hypothesis to explain the evolution of functionally
referential food-associated calls. Given the multiple functions of food-associated signals, we should not
expect a unitary explanation.
Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
A key question in the animal communication literature concerns
whether animal signals convey information to receivers about
objects or events in the external world (Seyfarth & Cheney 2003;
Seyfarth et al. 2010; but see Rendall et al. 2009). These signals,
termed ‘functionally referential’, have been defined as those that
enable receivers to predict environmental events in the absence of
other visual or contextual cues, to the extent that the signal elicits
the same adaptive response in the receivers as if the receivers had
actually experienced the eliciting stimuli themselves (Marler et al.
1992; Macedonia & Evans 1993; Evans 1997). The use of the
modifier ‘functional’ acknowledges the fact that, although some
animals produce calls that appear to refer to external objects or
events, the psychological processes underlying call production and
perception are poorly understood (Marler et al. 1992). This definition further takes into account that, at least from the producer’s
* Correspondence: Z. Clay, Living Links, Emory University, 36 Eagle Row, Atlanta,
GA 30322, U.S.A.
E-mail address: [email protected] (Z. Clay).
perspective, these calls in nonhuman animals differ substantially
from truly referential communication in the linguistic sense. A key
difference is that animal signallers appear to lack the flexibility and
communicative intentions seen in language, with calls more
genetically predetermined (e.g. Zuberbühler 2003; Seyfarth &
Cheney 2010). Nevertheless, functionally referential vocalizations
continue to arouse considerable interest and debate because of
their implications for the evolution of symbolic communication
and language (e.g. Scarantino 2010), as well as for indicating that
some aspects of animal communication may be conceptually,
rather than just affectively or emotionally, driven (Cheney &
Seyfarth 1990; Zuberbühler et al. 1999).
Using the original terminology, a signal must meet specific
production and perception criteria to be classified as functionally
referential (Seyfarth et al. 1980; Marler et al. 1992; Macedonia &
Evans 1993; Evans 1997). First, the signal must possess a discrete
acoustic structure and be stimulus-class specific (i.e. there must be
a tight association between signal production and the eliciting
stimuli). Second, the signal must elicit the appropriate receiver
response, independent of context (Marler et al. 1992; Evans et al.
0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2011.12.008
Please cite this article in press as: Clay, Z., et al., Food-associated vocalizations in mammals and birds: what do these calls really mean?, Animal
Behaviour (2012), doi:10.1016/j.anbehav.2011.12.008
2
Z. Clay et al. / Animal Behaviour xxx (2012) 1e8
1993; Evans 1997). Following this definitive framework, functionally referential vocalizations have been identified in many, but not
all, primate species (see Zuberbühler 2003, 2009), as well as in
bird and other mammalian species, such as fowl, Gallus gallus
(Evans & Marler 1994; Evans & Evans 1999), ravens, Corvus corvax
(Bugnyar et al. 2001), black-capped chickadees, Poecile atricapillus
(Templeton et al. 2005) and meerkats, Suricata suricatta (Manser
et al. 2001). To date, the majority of evidence for functionally
referential signals comes from studies of alarm call systems
(Zuberbühler 2003, 2009). Using a combination of observational
studies and playback experiments, alarm calls have been shown to
convey a range of information about the predation event, including
the class of predator (e.g. terrestrial or aerial), level of response
urgency and the caller’s imminent behaviour (Evans 1997;
Blumstein 1999; Leavesley & Magrath 2005).
However, although such signals have the potential to provide
information about specific events in the environment, a growing
body of evidence suggests that most alarm signals do not meet the
strict definition for production specificity. For example, evidence
from a range of species has shown that alarm calls produced to
specific predator types may also be given in other circumstances,
including in response to nonpredatory disturbances (i.e. falling
trees and nonpredatory animals: Arnold & Zuberbühler 2006;
Wheeler 2010), and in response to social disturbances, such as
agonistic encounters with other conspecific groups (Fichtel &
Kappeler 2002; Digweed et al. 2005; Fichtel & van Schaik 2006),
as well as during habitual dawn choruses (Marler 1972). Rather
than conveying highly specific information to receivers, these calls
may function to attract the attention of the receiver to a particular
stimulus (K. Arnold & K. Zuberbühler, unpublished data). This
evidence suggests that the many animal signals that convey information have a broader use and may not meet the original definition
of functionally referential. This matter will be further discussed in
later sections.
In addition to alarm call systems, vocalizations produced during
feeding have also been identified as functionally referential in
a number of bird and mammal species (e.g. fowl: Evans & Evans
1999; ravens: Bugnyar et al. 2001; tufted capuchins, Cebus apella:
Di Bitetti 2003; rhesus macaques, Macaca mulatta: Hauser & Marler
1993a; chimpanzees: Slocombe & Zuberbühler 2005; Geoffroy’s
tufted-ear marmosets, Callithrix geoffroyi: Kitzmann & Caine 2009).
The possibility of referential signals in the feeding context follows
from the logic that, in a manner similar to that of alarm calls, foodassociated calls are elicited by specific stimuli that occur within the
external environment (i.e. the discovery or presence of food).
In this review, we ask whether food-associated calls in a range of
species meet the criteria for functional reference and address the
question of the potential evolutionary drivers for food-associated
calls. The key question is whether, similar to alarm calls, there
may be a unifying explanation to food-associated calls. To investigate the possibility of functional reference, we will explore the
kinds of information conveyed by food-associated calls, and their
referential specificity and underlying functions.
FUNCTIONALLY REFERENTIAL FOOD-ASSOCIATED CALLS?
To date, the most convincing cases of functional reference in the
feeding context come from studies of fowl (Evans & Marler 1994;
Evans & Evans 1999, 2007). Upon discovery of a food item in the
presence of a hen, male fowl produce a specific food-associated
vocalization. Consistent with the criteria described above, fowl’s
food-associated calls are produced specifically within the context of
food, have an acoustically distinct structure, and playback experiments have demonstrated that they elicit specific feeding behaviours in receivers, in the absence of other stimuli (Marler et al. 1986;
Evans & Marler 1994; Evans & Evans 1999). Beyond fulfilling the
production criteria, results from a playback study by Evans & Evans
(2007) indicated that receivers perceive these calls as food specific
and that these calls appear to create a representation of food in the
receiver.
Similarly, a recent study of marmosets (Callithrix geoffroyi)
showed that receivers increased feeding-related behaviours
(foraging and feeding) following playbacks of food-associated calls
compared to when they heard control vocalizations (Kitzmann &
Caine 2009). Playback experiments with both chimpanzees, Pan
troglodytes, and bonobos, Pan paniscus, have demonstrated that
receivers expend greater foraging effort (e.g. time spent foraging,
number of inspections of a feeding patch) following playbacks of
food-associated calls as opposed to control conditions, where no
sounds were played (Slocombe & Zuberbühler 2005; Clay &
Zuberbühler 2011). Receivers also exerted a greater foraging
effort at the location associated with the specific type of foodvocalization played (i.e. calls associated with high- versus lowquality foods). However, in both studies, the individuals were
required to first learn the contingency that food ‘could’ be available
in one of two previously learned feeding locations. Thus, although
individuals in both studies increased foraging effort at the location
associated with the call, their previous experience makes it difficult
to completely rule out the possibility that, upon hearing the calls,
individuals were responding to caller arousal rather than to information regarding food presence specifically.
In other playback studies, the perceptual responses of receivers
have been measured in terms of approach behaviour and time
spent looking towards the speaker playing the food-associated calls
(e.g. Di Bitetti 2003; Gros-Louis 2004a). However, while a greater
approach response could feasibly result from an expectation of food
presence, approach behaviours themselves are not equivalent to
feeding behaviours. Approaching the playback speaker may instead
indicate that the calls are effective in social recruitment or in
communicating the caller’s level of excitement, neither of which is
necessarily related to food. In this manner, many of the studies
claiming functional reference have still not provided conclusive
evidence fulfilling the perception criteria that such calls refer to
specific feeding opportunities in the environment. And, unlike
predator-class-specific alarm calls, in these cases, referential foodassociated calls may only communicate that food is present, rather
than conveying additional information about the event, such as
food type or quantity.
FOOD-ASSOCIATED VERSUS FOOD-SPECIFIC VOCALIZATIONS
Acoustic specificity between stimulus and signal, such as has
been demonstrated for fowl food calls, is a key prerequisite for
functional reference. The notable problem for a unifying concept of
functionally referential food-associated calls is that, for a considerable number of species, calls produced during feeding are also
produced in nonfood contexts (e.g. toque macaque, Macaca sinica:
Dittus 1984; spider monkey, Ateles geoffroyi: Chapman & Lefebvre
1990; rhesus macaque, Macaca mulatta: Hauser & Marler, 1993a;
golden-lion tamarin, Leontopithecus roaslia: Halloy & Kleiman 1994;
red-bellied tamarin, Saguinus labiatus: Roush & Snowdon 2000;
bonobo: Clay & Zuberbühler 2009), and in some species, may not
even be food-specific at all (greater spear-nosed bat, Phyllostomus
hastatus: Wilkinson & Boughman 1998; bottlenose dolphin,
Tursiops truncates: Janik 2000; pinyon jay, Gymnorhinus cyanocephalus: Dahlin et al. 2005). For example, spider monkey ‘whinnie’
calls attract foragers to the food source but also serve other functions in social recruitment that are unrelated to feeding (Chapman
& Lefebvre 1990). Greater spear-nosed bats produce contact calls
that function, in the feeding context, to recruit conspecifics to the
Please cite this article in press as: Clay, Z., et al., Food-associated vocalizations in mammals and birds: what do these calls really mean?, Animal
Behaviour (2012), doi:10.1016/j.anbehav.2011.12.008
Z. Clay et al. / Animal Behaviour xxx (2012) 1e8
feeding site (Wilkinson & Boughman 1998). Golden-lion tamarins
produce the ‘chuck’ call during feeding but also during intergroup
encounters and predator mobbing (Halloy & Kleiman 1994). Toque
macaques produce a specific call in response to food; however, they
also sometimes produce this call during nonfood contexts associated with elation, such as at the onset of rain following dry periods,
or on hot sunny days towards the end of the rainy season (Dittus
1984). Thus, although such calls may be associated with feeding,
their production within nonfood contexts indicates that these calls
may function more generally in social recruitment and may more
accurately reflect the caller’s motivational response to an event
rather than the caller’s discovery of food specifically.
3
a function of distance to the food source; von Frisch 1956), it is
relevant to note that there are no examples of functionally referential alarm calls in which information is conveyed via call rates
alone (Blumstein 1999). Instead, most animals produce acoustically
distinct alarm calls that convey referential information about
specific features of the predation event, such as the class of predator or the response urgency (Evans et al. 1993; Blumstein 1999;
Zuberbühler 2003). Therefore, although call rate may provide
some information about the feeding event, the degree of specificity
may be insufficient in the majority of species examined to be
classed as functionally referential with regard to the specific characteristics of the feeding opportunity, such as food quality, divisibility or accessibility.
WHAT INFORMATION DO FOOD-ASSOCIATED CALLS CONVEY?
ACOUSTIC VARIATION IN FOOD-ASSOCIATED CALLS
Related to the question of acoustic specificity is determining
what information may be conveyed by food-associated calls. The
arousal-based perspective suggests that food-associated calls most
likely relate to the signaller’s level of excitement or arousal in
response to the feeding event (e.g. Owren & Rendall 2001). In this
sense, receivers may be responding to the signaller’s increased level
of excitement, which has been triggered by the presence of food,
rather than the specific expectation of a feeding opportunity.
However, disentangling motivation from reference is notoriously
difficult to address empirically, although it is likely that both may
be communicated (Evans 1997). This follows from a series of
studies that have shown that even vocal signals with high
emotional valence, such as alarm calls, can still simultaneously
communicate referential information about an external object or
event (see Seyfarth et al. 2010). For instance, recent work on the
alarm call responses of meerkats has demonstrated that both
emotional and referential information are coded into the same
signal and that they develop on different ontogenetic timescales
(Hollen & Manser 2007). Furthermore, it can also be the case that
a call that, from the signaller’s perspective, is purely arousal based
may still provide potentially functionally referential information if
the call can be shown to be elicited by a narrow range of stimuli.
The issue of disentangling arousal from reference may be less
problematic if the question of the information conveyed by a signal
is addressed separately from both the signaller’s and receiver’s
perspectives (Seyfarth & Cheney 2003).
Therefore, while food-associated calls undoubtedly convey
some degree of information of the caller’s level of arousal in
response to the presence of food, there is also the potential for foodassociated calls to provide other information, including the quantity, quality or divisibility of the food source (see Table 1 for details).
For the majority of species, this additional information about the
feeding opportunity appears to be conveyed via changes in call rate,
rather than changes in the acoustic structure of the calls themselves. For example, tufted capuchins and chimpanzees increase
the call rate in response to greater quantities of foods (Hauser et al.
1993; Di Bitetti 2005), while male fowl (Marler et al. 1986), cottontop tamarins, Saguinus oedipus (Elowson et al. 1991), red-bellied
tamarins, Saguinus labiatus (Caine et al. 1995) and spider monkeys
(Chapman & Lefebvre 1990) increase their call rates in response to
both greater quantities of food and foods of higher quality. Changes
in call rate have also been shown to covary with other features
relating to the caller’s perception of the feeding event, including
food divisibility (Hauser et al. 1993), food accessibility (Bugnyar
et al. 2001), the anticipation of food acquisition (Gros-Louis
2006), as well as the caller’s hunger level (Hauser & Marler
1993a; Wauters et al. 1999).
Although changes in call rates may feasibly represent a form of
functionally referential communication (e.g. in the waggle dance of
the honeybee, Apis mellifera, the length of the waggle run varies as
Although variation in call rate is the most common form of
acoustic variation in food-associated signalling, some species
produce food-associated calls whose acoustic structure covaries
with features of the feeding event (golden-lion tamarins: Benz
1993; rhesus macaques: Hauser & Marler, 1993a; ravens: Bugnyar
et al. 2001; chimpanzees: Slocombe & Zuberbühler 2006; bonobos: Clay & Zuberbühler 2009). Furthermore, playback experiments
in some of these species have also demonstrated that these acoustic
variants are meaningful to receivers (Hauser 1998; Slocombe &
Zuberbühler 2005; Clay & Zuberbühler 2011).
One striking similarity across studies is that acoustic variation in
food-associated calls is typically associated with perceived food
quality, rather than other food-specific features such as quantity or
divisibility (but see Bugnyar et al. 2001). Chimpanzees, for example,
produce graded variants of their food-associated ‘rough grunt’ as
a function of food quality (Slocombe & Zuberbühler 2006), whereas
bonobos produce an array of different food-associated calls whose
production is probabilistically related to the quality of food
encountered by the caller (Clay & Zuberbühler 2009). Rhesus
macaques produce up to five food-associated calls; three calls
(‘warble’, ‘harmonic arch’, ‘chirp’) are given in response to highquality and rare food items, whilst the other two calls (‘coos’,
‘grunts’) are given to lower-quality foods as well as in nonfood
contexts (e.g. group movement, grooming; Hauser & Marler 1993a).
In a habituationedishabituation playback experiment, Hauser
(1998) found that rhesus monkeys categorized food-associated
calls based upon their referential similarities rather than shared
acoustic features, indicating that call perception is based on their
functional referents rather than purely on acoustic features.
One obvious question is why this select group of species, but
apparently not other species, communicate about food quality via
acoustic characteristics instead of by call rate. However, referential
alarm calls are not an ideal model for understanding the presence
or absence of referentiality in food-associated calling. For instance,
while there is compelling evidence that the evolution of referential
alarm calls is driven by the incompatibility of escape responses
(Macedonia & Evans 1993; but see earlier discussion for cases
where escape strategies are not incompatible or not the usual
reaction to alarm calls: e.g. Fichtel & Kappeler 2002; Digweed et al.
2005; Wheeler 2008), feeding poses no such incompatibility
problem. Perhaps the closest analogy to alarm calls is that seen
when a social species encounters divisible versus indivisible food.
Yet even here, the trend seems to be to elect to produce or not to
produce a food call, rather than to produce variable food-associated
calls (e.g. Dahlin et al. 2005; Table 1).
In addition to food quality, acoustic structure can also relate to
other, more social features of the feeding event. For instance, ravens
produce both short ‘who’ and long ‘haa’ yells during feeding and
their differential usage is relative to food availability (Bugnyar et al.
Please cite this article in press as: Clay, Z., et al., Food-associated vocalizations in mammals and birds: what do these calls really mean?, Animal
Behaviour (2012), doi:10.1016/j.anbehav.2011.12.008
4
Species
Specificity of production
(in food context)
Receiver response
Changes in call with
food characteristics
Information encoded by
food-associated calls
Social group
structure
Source
Fowl
Gallus gallus
House sparrow
Passer domesticus
Pinyon jay
Gymnorhinus cyanocephalus
Yes
Increased call rate
Quality of food
Stable
Yes
Approach and
foraging behaviour
Approach
None
Divisibility of food
Transient
Marler et al. 1986;
Evans & Evans 1999
Elgar 1986
No
Approach
Number of calls and use
of call groups vs single calls
Variable, dependent
on season
Dahlin et al. 2005
Cliff swallow
Petrocheldion pyrrhonota
Carolina chickadee
Poecile carolinensis
Raven
Corvus corvax
Yes
Approach
None
Transient
Brown et al. 1991
Yes (for D call)
Approach
Number of calls
Social recruitment: call
when alone to attract
foragers and call more
in presence of mate
Quantity of food (insect
swarm density)
Social recruitment
Transient
Mahurin & Freeberg 2009
Yes
Approach
Increased call rate
(‘haa’ calls but not ‘yells’)
FissioneFusion
Heinrich 1988; Bugnyar et al. 2001
Greater spear-nosed bat
Phllostomus hastatus
No
Approach
None
Stable
Wilkinson & Boughman 1998
Bottlenose dolphin
Tursiops truncates
No
Approach
Not specified in
the literature
FissioneFusion
Janik 2000
Marmoset
Callithrix geoffroyi
Chimpanzee
Pan troglodytes
Yes
Approach and
foraging behaviour
Approach and
foraging behaviour
Not specified in
the literature
Increased call rate,
distinct sounds
(‘rough grunts’)
Distinct sounds
Stable
Kitzmann & Caine 2009
FissioneFusion
Bonobo
Pan paniscus
Tufted capuchin monkey
Cebus apella nigritus
White-faced capuchin monkey
Cebus capucinus
Yes
Quantity/divisibility/
quality of food,
resource ownership
Quality of food
Stable
Hauser & Wrangham 1987;
Hauser et al. 1993;
Slocombe & Zuberbühler 2006
Clay & Zuberbühler 2009, 2011
Yes
Approach site previously
associated with food
Approach
Increased call rate
Quantity/quality of food
Stable
Di Bitetti 2003, 2005
Yes
Approach
Increased call rate
Stable
Boinski & Campbell 1996;
Gros-Louis 2004a, b, 2006
Red-bellied tamarin
Saguinus labiatus
Yes
Approach implied but
not directly tested
Increased call rate
Stable
Caine et al. 1995
Spider monkey
Ateles geoffroyi
Cottontop tamarin
Saguinus oedipus
No
Approach
Increased call rate
Stable
Chapman & Lefebvre 1990
No
Food call
Increased call rate,
call type (C- and D-chirp)
Stable
Elowson et al. 1991;
Roush & Snowdon 2000
Golden-lion tamarin
Leontopithecus rosalia
Mandrill
Mandrillus sphinx
No (predator mobbing,
intergroup interactions)
Yes
Context dependent
Call rate and
distinct sounds
Not tested
Caller spacing, resource
ownership, anticipation
of food acquisition
Quantity/quality of food,
caller spacing, resource
ownership, social
recruitment
Social recruitment,
quantity/quality of food
Quantity/quality of food,
caller food preference,
approaching food, feeding
Quality of food, caller
food preference
Social recruitment
Stable
Benz et al. 1992; Benz 1993
Laidre 2006
Rhesus macaque
Macaca mulatta
No (group movement,
grooming, mother-infant
interactions)
No (rain after drought)
Stable/male
membership
changes with season
Stable
Stable
Dittus 1984, 1988
Toque macaque
Macaca sinica
Yes
Accessibility, caller’s
hunger level and
quality of food
Social recruitment:
contact calls used
during foraging
for coordination
Food presence,
exploit prey sensory
system to facilitate
capture
Social recruitment
Approach
Context dependent
Distinct sounds (chirps,
warbles, harmonic arches)
Context dependent
Probability of calling
Divisibility of food,
caller’s hunger level,
caller food preference
Quantity/rarity/
quality of food
Hauser & Marler 1993a, b
Z. Clay et al. / Animal Behaviour xxx (2012) 1e8
Please cite this article in press as: Clay, Z., et al., Food-associated vocalizations in mammals and birds: what do these calls really mean?, Animal
Behaviour (2012), doi:10.1016/j.anbehav.2011.12.008
Table 1
Summary of the results of studies of food-associated calls in mammals and birds, from caller and receiver perspectives
Z. Clay et al. / Animal Behaviour xxx (2012) 1e8
2001). ‘Haa’ yells are produced upon sighting the food and appear
to provide information about the food itself and its accessibility.
However, ‘who’ yells are produced upon approaching the food and
appear to convey information about the caller during the feeding
event. Carolina chickadees, Poecile carolinensis, adjust the acoustic
structure of their calls depending on whether another individual
has joined them to feed. Playback experiments show that these
calls function in social recruitment to a feeding site compared to
calls given after other individuals have joined the caller (Mahurin &
Freeberg 2009). Food-associated calls may also convey information
about the caller themselves, including the caller’s rank (cottontop
tamarins: Roush & Snowdon 1999), identity or sex (white-faced
capuchins, Cebus capucinus: Gros-Louis 2006).
WHAT IS THE FUNCTION OF FOOD-ASSOCIATED CALLS?
Along with the information conveyed by food-associated calls,
an important related question concerns the ultimate function of
these calls. Although this is a discrete question, logically separate
from the meaning of food calls, an integrative Tinbergian approach
to understanding the phenomena warrants some discussion of
function. Indeed, by understanding the function of these calls, we
may evaluate the question of whether there is a unifying explanation for the evolution of functionally referential food calls.
In their original synthesis, Macedonia & Evans (1993) focused
only on the putative call ‘meaning’ when developing a unifying
hypothesis for functional referential vocalizations. However,
incorporating call function can provide insights into cases for
acoustically distinct calls (i.e. alarm or food-associated calls) where
response strategies are not necessarily incompatible (i.e. predator
escape strategies in response to predator-specific alarm calls) or
may differ from the typical behavioural reaction to the calls (e.g.
Kirchhoff & Hammerschmidt 2006; Furrer & Manser 2009).
Similarly to alarm calls (e.g. Wheeler 2008), there appear to be
a diverse array of possible functions to food-associated calls.
Several themes have emerged in our review, and although not
mutually exclusive, they indicate that the function of foodassociated calls is closely tied to the socioecology of a given
species. For the majority of species, food-associated calls attract
foragers and appear to function in social recruitment (e.g. Dittus
1984; Chapman & Lefebvre 1990; but see Gros-Louis 2004b;
Table 1). Although social recruitment to a food source may, at first,
appear counterintuitive, there are a number of benefits to attracting
other individuals to the food source. This may work at the level of
enhancing inclusive fitness via kin selection (e.g. Hauser & Marler
1993a, b; Judd & Sherman 1996) as well as by enhancing fitness
directly.
For small-bodied species that are vulnerable to predation,
recruiting conspecifics, or even heterospecifics, may function to
reduce predation risk, either by dilution or increased vigilance
(Sridhar et al. 2009; house sparrows, Passer domesticus: Elgar 1986;
Newman & Caraco 1989; Elowson et al. 1991; cottontop tamarins:
Caine et al. 1995). For flocking bird species, attracting conspecifics
may also benefit the forager in terms of manipulation of the food
patch. For example, in colonially nesting cliff swallows, Petrochelidon pyrrhonota, that feed on insect swarms, attracting more
foragers may increase the chance of the insect swarm’s movements
being tracked, thus enabling each signaller to exploit the same
insect swarm for longer than if these signallers were foraging alone
(Brown et al. 1991). In other species, callers may benefit by
recruiting foragers that can assist in the cooperative defence of
resources (Heinrich & Marzluff 1991; Marzluff & Heinrich 1991;
Wilkinson & Boughman 1998).
In addition to functions relating to defence, signallers may
receive reproductive rewards by attracting conspecifics to the food
5
source. Male fowl call more often in the presence of females (Marler
et al. 1986; Evans & Marler 1994), and females in turn prefer to mate
with males that food call more often (Pizzari 2003). Likewise, the
production of food-associated calls by male bonobos attract
females to a food source, which subsequently engage in copulations
with the calling males (Van Krunkelsven et al. 1996). Reproductive
benefits may also work at the level of maintaining an association
with long-term mating partners. For instance, pinyon jays call more
when their long-term mate is present than when nonmates are
present (Dahlin et al. 2005). In addition to direct reproductive
benefits, signallers may also receive indirect benefits, through kin
selection, by alerting kin to a food patch (Hauser & Marler 1993a, b;
Judd & Sherman 1996). For example, tufted capuchins call more in
the presence of larger audiences of kin than of nonkin (Pollick et al.
2005), and in rhesus macaques, females in larger matrilines call
more than those in smaller matrilines (Hauser & Marler 1993a).
The attraction of potential mates indicates that food-associated
calls may play a role in enhancing social status or reputation. The
communication of social status is also supported by evidence that
food calls may also function to attract allies and close social partners (e.g. bonobos: Van Krunkelsven et al. 1996; chimpanzees:
Slocombe et al. 2010). This ‘reputation building’ function may be
especially relevant in species living in socially stable groups with
the chance for repeated interactions between group members (as
opposed to transient group formations, such as flocking birds or
bats). In a recent study by Slocombe et al. (2010), male chimpanzees
were shown to call more in the presence of close social partners,
regardless of the audience size or the presence of oestrous females.
Furthermore, although the size and divisibility of the food patch
influenced calling, the presence of social partners explained most of
the variation in calling behaviour, suggesting that food-associated
calls may function to enhance affiliation between allies. It is also
notable that in chimpanzees and bonobos, there appears to be an
association between acoustically variable calls signalling food
quality and the suggestion of a ‘reputation’ building function. Such
a hypothesis requires further attention.
In contrast to these previous examples in which food-associated
calls function in social recruitment, food calls may function to
reduce foraging competition in some primate species that forage in
large and stable groups (rhesus macaques: Hauser & Marler 1993a,
b; cottontop tamarins: Caine et al. 1995; white-faced capuchins:
Gros-Louis 2004b; tufted capuchins: Di Bitetti 2005). Conflicts
resulting from competition over food are common in social
foragers, and thus food calling may provide a clear establishment of
resource ownership and the motivational state of the caller to
defend the resource, thereby reducing the likelihood of the caller
being challenged by another individual.
The best evidence in support of this function for food-associated
calling comes from white-faced capuchins (Gros-Louis 2004b) and
red-bellied tamarins (Caine et al. 1995). For both species, individuals that called were less likely to have food taken from them than
were individuals that remained silent. In white-faced capuchins,
call production increases the distance between foragers, thus
functioning to regulate forager spacing and reduce competition
(Boinski & Campbell 1996; Gros-Louis 2004b). In this species,
neither increased quantity nor divisibility of food increases the
likelihood of call production (Gros-Louis 2004b). Thus, for these
two species, food-associated calling may convey information to
potential challengers about the caller’s willingness to defend
their resource, thus deterring the challenger, and hence reducing
the likelihood of aggression following conflict over ownership
(Gros-Louis 2004b).
An alternative explanation to this ‘resource ownership’
hypothesis is that individuals call to avoid aggression from more
dominant individuals upon their discovery of food (Hauser et al.
Please cite this article in press as: Clay, Z., et al., Food-associated vocalizations in mammals and birds: what do these calls really mean?, Animal
Behaviour (2012), doi:10.1016/j.anbehav.2011.12.008
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Z. Clay et al. / Animal Behaviour xxx (2012) 1e8
1993). In rhesus macaques, a species with strict dominance hierarchies, Hauser & Marler (1993b) found that individuals that did
not call upon finding food were more likely to receive aggression
from other group members than those that did vocalize. The
possibility that group members call to avoid ‘punishment’ implies
the unlikely scenario that monkeys are capable of some degree of
mental state attribution, in the sense that the more dominant
individual expects to be informed and that they are aware that
information has been withheld from them. This kind of hypothesis
does not appear likely based on the current evidence for primates,
aside from possibly great apes (e.g. Cheney & Seyfarth 1996, 1999;
Hare et al. 2001). It may be more parsimonious to conclude that
animals may be using more simple associations; for instance: expel
from the food patch those subordinates that do not call, but cofeed
with those that do call. In either case, the function of foodassociated calls in this instance may be to reduce aggression
during feeding or to facilitate group cohesion.
With some notable exceptions, the proximate function of foodassociated calling may be to attract other individuals to the feeding
opportunity. However, the ultimate function varies with the social
and ecological pressures faced by the species in question. For
groups with stable or semi-stable social foraging groups, the
functions include facilitation of group cohesion, consolidation of
social alliances, enhancement of social status within the group, as
well as increased direct and indirect fitness. However, not all of
these functions are present in all species with stable social groups.
In species with more transient group composition, such as
flocking birds, the function of food calls may be to reduce predation
threat and time spent vigilant and to increase foraging efficiency
(Sridhar et al. 2009). However, small-bodied mammals with stable
social groups face similar pressures (e.g. red-bellied tamarins:
Caine et al. 1995; greater spear-nosed bats: Wilkinson & Boughman
1998). In these species, food calls may share the same function as in
species with more fluid group membership.
Based on the evidence detailed above, it seems unlikely that
there is a generalized or unified function to food-associated calls.
The function of food-associated calls depends on the balance of
social and ecological pressures faced by a given species. Yet, social
and ecological pressures do not appear to determine which species
produce functionally referential food signals (Table 1). There is
evidence from many species with stable, semi-stable and
completely transient social groups that food-associated calls occur
in nonfeeding contexts and therefore do not meet the production
criteria for functionally referential calls. The majority of the species
in which both the production and perception criteria for functional
reference have been examined have stable social groups. However,
differences in the experimental methods used create a challenge for
conclusively determining whether food-associated calls in
a particular species should be classified as functionally referential
or only food-associated. Although the majority of the studies have
used playback experiments either in wild- or captive-living groups,
the control vocalizations selected range from very similar sounds
naturally produced by the species in question to no sounds played
(silence). In addition, the receiver response criteria used to class
a call as functionally referential range from specific food-searching
behaviour to approach of the playback speaker. Some standardization of the methods used to evaluate putative functionally
referential signal is desirable, although this may be difficult to
achieve given the diversity of animals, information content and
functions of these signals.
CONCLUSIONS
The widespread evidence of selective food-associated signalling
suggests that, compared to other contexts in which functionally
referential signals have been identified (i.e. alarm or agonistic
interactions), food-associated calls may be produced or withheld in
response to the signaller’s own ecological, social and reproductive
pressures. The contrast between the production of alarm signals
and food-associated calls may reflect the difference in the pressures
that would have selected for functionally referential signals. Alarm
signals have a critical function in survival, whereas food-associated
calls do not. The pressure for alarm calls to convey accurate and
actionable information to increase mate or other kin survival has
most likely selected for their referential function. Food-associated
calling has not been so tightly linked to reproductive success or
survival; therefore, there may be less selective pressure for the
caller to provide specific information about feeding opportunities.
Evidence from a range of taxa suggests that the variability and
specificity of food-associated call production will most likely be
linked to the social structure and environmental factors affecting
each species. In species that live in stable social groups, which
enable repeated interactions over time, the selective use of foodassociated calls may be more likely to function to enhance
a caller’s social status. However, competition for resources in large
stable foraging groups may instead select for food-associated calls
that advertise resource ownership and function to reduce antagonistic interactions. Predation risk and resource defence are also
factors affecting the use of food-associated calls, and appear most
relevant for smaller-bodied species under strong predation pressure. In these instances, food-associated calls function to recruit
conspecifics to the food source.
Yet, even species that we might expect to give food calls do not
produce them. For instance, macaques often give ‘coo’ calls in
response to food (Hauser & Marler 1993a), but no one has ever
described or noted analogous ‘food-associated’ calls in vervet
monkeys or baboons. This is a puzzle, given these species’ many
behavioural similarities and their rather similar ecology. A welldeveloped theory of food-associated calling should explain both
the presence and the absence of food calls.
Taken together, the evidence does not suggest a unifying
explanation for functionally referential food-associated signals.
Instead, it suggests that a suite of factors affecting each species will
determine under what circumstances food-associated calls are
produced and what information is conveyed. Signals during feeding
may have the potential to convey a considerable amount of useful
information to receivers, but the evidence for their status as functionally referential signals is, aside from a few select cases, less
convincing.
Acknowledgments
This paper emerged from a meeting, Vocal Communication and
Social Cognition, organized by Marta Manser and Simon Townsend,
and supported by the Gleichstellung, University of Zurich. Z.C. was
supported by The Leverhulme Trust, with many thanks to Prof. K.
Zuberbühler. D.T.B. was supported by National Science Foundation
grant NSF IDBR-0754247. We thank Dorothy Cheney and two
anonymous referees for their particularly insightful comments.
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